Interventricular comparison of the energetics of contraction of trabeculae carneae isolated from the rat heart

Journal of Physiology

Volumn 591, Issue 3, 2013, Pages 701-717

  Han, June Chiew ^a   Taberner, Andrew J ^a,b   Nielsen, Poul M F ^a,b   Loiselle, Denis S ^a,b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; BIOMECHANICS; CALORIMETER; CALORIMETRY; CONTROLLED STUDY; ENERGY TRANSFER; ENTHALPY; HEART; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE; HEART MUSCLE METABOLISM; HEART RIGHT VENTRICLE FUNCTION; HEART TRABECULAE CARNEAE; HEART VENTRICLE CONTRACTION; HEART VENTRICLE PRESSURE; HEART VOLUME; ISOLATED HEART; MALE; MUSCLE STRESS; NONHUMAN; PRIORITY JOURNAL; RAT; THERMOGENESIS;

ANIMALS; CALORIMETRY; ENERGY METABOLISM; HEART VENTRICLES; HOT TEMPERATURE; MALE; MYOCARDIAL CONTRACTION; RATS; RATS, WISTAR; STRESS, PHYSIOLOGICAL; VENTRICULAR FUNCTION;

EID: 84873169932     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.242719     Document Type: Article

References (107)

1. Afzal N & Dhalla NS (1992). Differential changes in left and right ventricular SR calcium transport in congestive heart failure. Am J Physiol Heart Circ Physiol 262, H868-H874.
2. Asanoi H, Sasayama S & Kameyama T (1989). Ventriculoarterial coupling in normal and failing heart in humans [published erratum appears in Circ Res 1990 Apr;66(4):1170]. Circ Res 65, 483-493.
3. Bárány M (1967). ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50, 197-216.
4. Barclay CJ (1996). Mechanical efficiency and fatigue of fast and slow muscles of the mouse. J Physiol 497, 781-794.
5. Barclay CJ (1999). A weakly coupled version of the Huxley crossbridge model can simulate energetics of amphibian and mammalian skeletal muscle. J Muscle Res Cell Motil 20, 163-176.
6. Barclay CJ & Widén C (2010). Efficiency of cross-bridges and mitochondria in mouse cardiac muscle. Adv Exp Med Biol 682, 267-278.
7. Barclay CJ, Widén C & Mellors LJ (2003). Initial mechanical efficiency of isolated cardiac muscle. J Exp Biol 206, 2725-2732.
8. Barclay CJ, Woledge RC & Curtin NA (2010a). Inferring crossbridge properties from skeletal muscle energetics. Prog Biophys Molr Biol 102, 53-71.
9. Barclay CJ, Woledge RC & Curtin NA (2010b). Is the efficiency of mammalian (mouse) skeletal muscle temperature dependent J Physiol 588, 3819-3831.
10. Baxi J, Barclay CJ & Gibbs CL (2000). Energetics of rat papillary muscle during contractions with sinusoidal length changes. Am J Physiol Heart Circ Physiol 278, H1545-H1554.
11. Bokník P, Unkel C, Kirchhefer U, Kleideiter U, Klein-Wiele O, Knapp J, Linck B, Lüss H, Ulrich Müller F, Schmitz W, Vahlensieck U, Zimmermann N, Jones LR & Neumann J (1999). Regional expression of phospholamban in the human heart. Cardiovasc Res 43, 67-76.
12. Brooks WW, Bing OHL, Blaustein AS & Allen PD (1987). Comparison of contractile state and myosin isozymes of rat right and left ventricular myocardium. J Mol Cell Cardiol 19, 433-440.
13. Burkhoff D, Kronenberg MW, Yue DT, Maughan WL, Hunter WC & Sagawa K (1987). Quantitative comparison of canine right and left ventricular isovolumic pressure waves. Am J Physiol Heart Circ Physiol 253, H475-H479.
14. Burkhoff D & Sagawa K (1986). Ventricular efficiency predicted by an analytical model. Am J Physiol Regul Integr Comp Physiol 250, R1021-R1027.
15. Burkhoff D, Yue DT, Franz MR, Hunter WC, Sunagawa K, Maughan WL & Sagawa K (1984). Quantitative comparison of the force-interval relationships of the canine right and left ventricles. Circ Res 54, 468-473.
16. Burns JW & Covell JW (1972). Myocardial oxygen consumption during isotonic and isovolumic contractions in the intact heart. Am J Physiol 223, 1491-1497.
17. 2 uptake during hemodilution and beta-adrenergic stimulation. Am J Physiol Heart Circ Physiol 265, H1769-H1777.
18. Daut J & Elzinga G (1988). Heat production of quiescent ventricular trabeculae isolated from guinea-pig heart. J Physiol 398, 259-275.
19. Daut J & Elzinga G (1989). Substrate dependence of energy metabolism in isolated guinea-pig cardiac muscle: a microcalorimetric study. J Physiol 413, 379-397.
20. de Tombe PP, Jones S, Burkhoff D, Hunter WC & Kass DA (1993). Ventricular stroke work and efficiency both remain nearly optimal despite altered vascular loading. Am J Physiol Heart Circ Physiol 264, H1817-H1824.
21. de Tombe PP & ter Keurs HE (1990). Force and velocity of sarcomere shortening in trabeculae from rat heart. Effects of temperature. Circ Res 66, 1239-1254.
22. 2+ transport in different areas of dog heart. Can J Physiol Pharmacol 58, 360-367.
23. Effron MB, Bhatnagar GM, Spurgeon HA, Ruano-Arroyo G & Lakatta EG (1987). Changes in myosin isoenzymes, ATPase activity, and contraction duration in rat cardiac muscle with aging can be modulated by thyroxine. Circ Res 60, 238-245.
24. Elzinga G, Piene H & de Jong J (1980). Left and right ventricular pump function and consequences of having two pumps in one heart. A study on the isolated cat heart. Circ Res 46, 564-574.
25. Elzinga G & Westerhof N (1991). Matching between ventricle and arterial load. An evolutionary process. Circ Res 68, 1495-1500.
26. Fan TH, Frantz RP, Elam H, Sakamoto S, Imai N & Liang CS (1993). Reductions of myocardial Na-K-ATPase activity and ouabain binding sites in heart failure: prevention by nadolol. Am J Physiol Heart Circ Physiol 265, H2086-H2093.
27. Frenzei H & Feimann J (1984). Age-dependent structural changes in the myocardium of rats. A quantitative light- and electron-microscopic study on the right and left chamber wall. Mech Ageing Develop 27, 29-41.
28. Gibbs CL & Gibson WR (1969). Effect of ouabain on the energy output of rabbit cardiac muscle. Circ Res 24, 951-967.
29. Gibbs CL & Gibson WR (1970). Energy production in cardiac isotonic contractions. J Gen Physiol 56, 732-750.
30. Gibbs CL, Mommaerts WFHM & Ricchiuti NV (1967). Energetics of cardiac contractions. J Physiol 191, 25-46.
31. Gibbs CL, Wendt IR, Kotsanas G, Young IR & Woolley G (1990). Mechanical, energetic, and biochemical changes in long-term pressure overload of rabbit heart. Am J Physiol Heart Circ Physiol 259, H849-H859.
32. +)-ATPase in the rat heart and the effects of induced right ventricular hypertrophy and feeding with digitalis, sodium, and potassium. Cardiovasc Res 4, 6-13.
33. Goo S, Joshi P, Sands G, Gerneke D, Taberner A, Dollie Q, LeGrice I & Loiselle D (2009). Trabeculae carneae as models of the ventricular walls: implications for the delivery of oxygen. J Gen Physiol 134, 339-350.
34. Goodman SN (1999). Toward evidence-based medical statistics. 2: The Bayes factor. Ann Int Med 130, 1005-1013.
35. Grover EJ, Morgan JP, Stambler BS & Gwathmey JK (1994). Uniformity of calcium channel number and isometric contraction in human right and left ventricular myocardium. Basic Res Cardiol 89, 139-148.
36. 2+ exchange activity. Circ Res 66, 1171-1177.
37. Gruver EJ, Morgan JP, Stambler BS & SGwathmey JK (1994). Uniformity of calcium channel number and isometric contraction in human right and left ventricular myocardium. Basic Res Cardiol 89, 139-148.
38. Han J-C, Taberner AJ, Kirton RS, Nielsen PMF, Archer R, Kim N & Loiselle DS (2011). Radius-dependent decline of performance in isolated cardiac muscle does not reflect inadequacy of diffusive oxygen supply. Am J Physiol Heart Circ Physiol 300, H1222-H1236.
39. Han J-C, Taberner AJ, Kirton RS, Nielsen PMF, Smith NP & Loiselle DS (2009). A unique micromechanocalorimeter for simultaneous measurement of heat rate and force production of cardiac trabeculae carneae. J Appl Physiol 107, 946-951.
40. Han J-C, Taberner AJ, Nielsen PMF, Kirton RS, Ward M-L & Loiselle DS (2010). Energetics of stress production in isolated cardiac trabeculae from the rat. Am J Physiol Heart Circ Physiol 299, H1382-H1394.
41. Han J-C, Taberner AJ, Tran K, Goo S, Nickerson DP, Nash MP, Nielsen PMF, Crampin EJ & Loiselle DS (2012a). Comparison of the Gibbs and Suga formulations of cardiac energetics: the demise of "isoefficiency". J Appl Physiol 113, 996-1003.
42. Han J-C, Taberner AJ, Tran K, Nickerson DP, Nash MP, Nielsen PMF, Crampin EJ & Loiselle DS (2012b). Relating components of pressure-volume area in Suga's formulation of cardiac energetics to components of the stress-time integral J Appl Physiol 113, 988-995.
43. He Z-H, Bottinelli R, Pellegrino MA, Ferenczi MA & Reggiani C (2000). ATP consumption and efficiency of human single muscle fibers with different myosin isoform composition. Biophys J 79, 945-961.
44. Hill TL (1974). Theoretical formalism for the sliding filament model of contraction of striated muscle. Part I. Prog Biophys Molec Biol 28, 267-340.
45. Hill TL (1975). Theoretical formalism for the sliding filament model of contraction of striated muscle. Part II. Prog Biophys Molec Biol 29, 105-159.
46. Hisano R & Cooper G (1987). Correlation of force-length area with oxygen consumption in ferret papillary muscle. Circ Res 61, 318-328.
47. Hoh JFY, McGrath PA & Hale PT (1978). Electrophoretic analysis of multiple forms of rat cardiac myosin: effects of hypophysectomy and thyroxine replacement. J Mol Cell Cardiol 10, 1053-1076.
48. Holroyd SM & Gibbs CL (1992). Is there a shortening-heat component in mammalian cardiac muscle contraction Am J Physiol Heart Circ Physiol 262, H200-H208.
49. Huxley AF (1957). Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7, 255-318.
50. Ishijima A, Kojima H, Funatsu T, Tokunaga M, Higuchi H, Tanaka H & Yanagida T (1998). Simultaneous observation of individual ATPase and mechanical events by a single myosin molecule during interaction with actin. Cell 92, 161-171.
51. Janssen PM & Hunter WC (1995). Force, not sarcomere length, correlates with prolongation of isosarcometric contraction. Am J Physiol Heart Circ Physiol 269, H676-H685.
52. Janssen PML, Stull LB, Leppo MK, Altschuld RA & Marban E (2003). Selective contractile dysfunction of left, not right, ventricular myocardium in the SHHF rat. Am J Physiol Heart Circ Physiol 284, H772-H778.
53. Khalafbeigui F, Suga H & Sagawa K (1979). Left ventricular systolic pressure-volume area correlates with oxygen consumption. Am J Physiol Heart Circ Physiol 237, H566-H569.
54. Kiriazis H & Gibbs CL (1995). Papillary muscles split in the presence of 2, 3-butanedione monoxime have normal energetic and mechanical properties. Am J Physiol Heart Circ Physiol 269, H1685-H1694.
55. Kiriazis H & Gibbs CL (2000). Effects of aging on the work output and efficiency of rat papillary muscle. Cardiovasc Res 48, 111-119.
56. Kiriazis H, Gibbs CL, Kotsanas G & Young IR (1992). Mechanical and energetic changes in short-term volume and pressure overload of rabbit heart. Heart Vessels 7, 175-188.
57. Kleid JJ, Tada M, Repke DI & Katz AM (1972). Myosins from rat right and left ventricles. Comparison of ATPase activities and light fragments released by 8 m-urea. J Mol Cell Cardiol 4, 625-632.
58. Kleiman RB & Houser SR (1988). Electrophysiologic and mechanical properties of single feline RV and LV myocytes. J Mol Cell Cardiol 20, 973-982.
59. Kondo RP, Dederko DA, Teutsch C, Chrast J, Catalucci D, Chien KR & Giles WR (2006). Comparison of contraction and calcium handling between right and left ventricular myocytes from adult mouse heart: a role for repolarization waveform. J Physiol 571, 131-146.
60. Krukenkamp I, Silverman N, Sorlie D, Pridjian A, Feinberg H & Levitsky S (1986). Oxygen utilization during isovolumic pressure-volume loading: effects of prolonged extracorporeal circulation and cardioplegic arrest. Ann Thorac Surg 41, 407-412.
61. Kusachi S, Nishiyama O, Yasuhara K, Saito D, Haraoka S & Nagashima H (1982). Right and left ventricular oxygen metabolism in open-chest dogs. Am J Physiol Heart Circ Physiol 243, H761-H766.
62. Landesberg A, Livshitz L & ter Keurs HEDJ (2000). The effect of sarcomere shortening velocity on force generation, analysis, and verification of models for crossbridge dynamics. Ann Biomed Eng 28, 968-978.
63. Little WC & Cheng CP (1991). Left ventricular-arterial coupling in conscious dogs. Am J Physiol Heart Circ Physiol 261, H70-H76.
64. Loiselle DS (1979). The effects of temperature on the energetics of rat papillary muscle. Pflugers Arch 379, 173-180.
65. Loiselle DS & Gibbs CL (1979). Species differences in cardiac energetics. Am J Physiol Heart Circ Physiol 237, H90-H98.
66. Mast F & Elzinga G (1988). Recovery heat production of isolated rabbit papillary muscle at 20 °C. Pflugers Arch 411, 600-605.
67. McMahon WS, Mukherjee R, Gillette PC, Crawford FA & Spinale FG (1996). Right and left ventricular geometry and myocyte contractile processes with dilated cardiomyopathy: myocyte growth and β-adrenergic responsiveness. Cardiovasc Res 31, 314-323.
68. Mellors LJ & Barclay CJ (2001). The energetics of rat papillary muscles undergoing realistic strain patterns. J Exp Biol 204, 3765-3777.
69. Mellors LJ, Gibbs CL & Barclay CJ (2001). Comparison of the efficiency of rat papillary muscles during afterloaded isotonic contractions and contractions with sinusoidal length changes. J Exp Biol 204, 1765-1774.
70. Mercadier JJ, Lompre AM, Wisnewsky C, Samuel JL, Bercovici J, Swynghedauw B & Schwartz K (1981). Myosin isoenzyme changes in several models of rat cardiac hypertrophy. Circ Res 49, 525-532.
71. Myhre ES, Johansen A, Bjornstad J & Piene H (1986). The effect of contractility and preload on matching between the canine left ventricle and afterload. Circulation 73, 161-171.
72. Obayashi M, Xiao B, Stuyvers BD, Davidoff AW, Mei J, Chen SRW & ter Keurs HEDJ (2006). Spontaneous diastolic contractions and phosphorylation of the cardiac ryanodine receptor at serine-2808 in congestive heart failure in rat. Cardiovasc Res 69, 140-151.
73. Pagani ED & Julian FJ (1984). Rabbit papillary muscle myosin isozymes and the velocity of muscle shortening. Circ Res 54, 586-594.
74. Piene H & Sund T (1982). Does normal pulmonary impedance constitute the optimum load for the right ventricle Am J Physiol Heart Circ Physiol 242, H154-H160.
75. Rosenfeld EV (2012). The interrelation between mechanical characteristics of contracting muscle, cross-bridge internal structure, and the mechanism of chemomechancial energy transduction. Eur Biophys J 41, 733-753.
76. Rouleau J, Paradis P, Shenasa H & Juneau C (1986). Faster time to peak tension and velocity of shortening in right versus left ventricular trabeculae and papillary muscles of dogs. Circ Res 59, 556-561.
77. Saito D, Tani H, Kusachi S, Uchida S, Ohbayashi N, Marutani M, Maekawa K, Tsuji T & Haraoka S (1991). Oxygen metabolism of the hypertrophic right ventricle in open chest dogs. Cardiovasc Res 25, 731-739.
78. Sandler H & Dodge HT (1963). Left ventricular tension and stress in man. Circ Res 13, 91-104.
79. Sands G, Goo S, Gerneke D, LeGrice I & Loiselle D (2011). The collagenous microstructure of cardiac ventricular trabeculae carneae. J Struct Biol 173, 110-116.
80. 2+-handling properties of sarcoplasmic reticulum in right and left ventricles of normal rat myocardium. Am J Physiol Heart Circ Physiol 291, H88-H96.
81. Satoh K, Matsu-ura T, Enomoto M, Nakamura H, Michikawa T & Mikoshiba K (2011). Highly cooperative dependence of sarco/endoplasmic reticulum calcium ATPase (SERCA) 2a pump activity on cytosolic calcium in living cells. J Biol Chem 286, 20591-20599.
82. Semafuko W & Bowie W (1975). Papillary muscle dynamics: in situ function and responses of the papillary muscle. Am J Physiol 228, 1800-1807.
83. Smith DA (1998). A strain-dependent ratchet model for [phosphate]- and [ATP]-dependent muscle contraction. J Muscle Res Cell Motil 19, 189-211.
84. Smith NP, Barclay CJ & Loiselle DS (2005). The efficiency of muscle contraction. Prog Biophys Mol Biol 88, 1-58.
85. Smolich JJ, Walker AM, Campbell GR & Adamson TM (1989). Left and right ventricular myocardial morphometry in fetal, neonatal, and adult sheep. Am J Physiol Heart Circ Physiol 257, H1-H9.
86. Sorhus V, Sys SU, Natas A, Demolder MJ & Angelsen BAJ (2000). Controlled auxotonic twitch in papillary muscle: a new computer-based control approach. Comput Biomed Res 33, 398-415.
87. Suga H (1990). Ventricular energetics. Physiol Rev 70, 247-277.
88. Suga H, Hayashi T & Shirahata M (1981a). Ventricular systolic pressure-volume area as predictor of cardiac oxygen consumption. Am J Physiol Heart Circ Physiol 240, H39-H44.
89. Suga H, Hayashi T, Shirahata M, Suehiro S & Hisano R (1981b). Regression of cardiac oxygen consumption on ventricular pressure-volume area in dog. Am J Physiol Heart Circ Physiol 240, H320-H325.
90. Syme DA (1994). The efficiency of frog ventricular muscle. J Exp Biol 197, 143-164.
91. Syrovy I, Delcayre C & Swynghedauw B (1979). Comparison of ATPase activity and light subunits in myosins from left and right ventricles and atria in seven mammalian species. J Mol Cell Cardiol 11, 1129-1135.
92. Taberner AJ, Han J-C, Loiselle DS & Nielsen PMF (2011). An innovative work-loop calorimeter for in vitro measurement of the mechanics and energetics of working cardiac trabeculae. J Appl Physiol 111, 1798-1803.
93. Taberner AJ, Hunter IW, Kirton RS, Nielsen PMF & Loiselle DS (2005). Characterization of a flow-through microcalorimeter for measuring the heat production of cardiac trabeculae. Rev Sci Instrum 76, 104901-104907.
94. Taylor TW, Goto Y & Suga H (1993). Variable cross-bridge cycling-ATP coupling accounts for cardiac mechanoenergetics. Am J Physiol Heart Circ Physiol 264, H994-H1004.
95. Toorop GP, Van den Horn GJ, Elzinga G & Westerhof N (1988). Matching between feline left ventricle and arterial load: optimal external power or efficiency. Am J Physiol Heart Circ Physiol 254, H279-H285.
96. van den Horn G, Westerhof N & Elzinga G (1985). Optimal power generation by the left ventricle. A study in the anesthetized open thorax cat. Circ Res 56, 252-261.
97. van den Horn GJ, Westerhof N & Elzinga G (1986). Feline left ventricle does not always operate at optimum power output. Am J Physiol Heart Circ Physiol 250, H961-H967.
98. Vendelin M, Bovendeerd PHM, Arts T, Engelbrecht J & van Campen DH (2000). Cardiac mechanoenergetics replicated by cross-bridge model. Ann Biomed Eng 28, 629-640.
99. Vendelin M, Bovendeerd PHM, Saks V & Engelbrecht J (2002). Cardiac mechanoenergetics in silico. Neuroendocrinol Lett 23, 13-20.
100. Winer BJ (1971). Statistical Principles in Experimental Design McGraw-Hill Book Company, New York
101. Woledge RC, Curtin NA & Homsher E (1985). Energetic Aspects of Muscle Contraction Academic Press, London
102. Woledge RC & Reilly PJ (1988). Molar enthalpy change for hydrolysis of phosphorylcreatine under conditions in muscle cells. Biophys J 54, 97-104.
103. Wong AYK & Rautaharju PM (1968). Stress distribution within the left ventricular wall approximated as a thick ellipsoidal shell. Am Heart J 75, 649-662.
104. Woods RH (1892). A few applications of a physical theorem to membranes in the human body in a state of tension. Trans R Acad Med Ireland: Section of Anatomy and Physiology 10, 417-327.
105. Yanagida T, Arata T & Oosawa F (1985). Sliding distance of actin filament induced by a myosin crossbridge during one ATP hydrolysis cycle. Nature 316, 366-369.
106. Yin FC (1981). Ventricular wall stress. Circ Res 49, 829-842.
107. Zong P, Tune JD & Downey HF (2005). Mechanisms of oxygen demand/supply balance in the right ventricle. Exp Biol Med 230, 507-519.